Biodegradability of Disinfectants in Surface Waters from Buenos Aires: Isolation of an Indigenous Strain Able to Degrade and Detoxify Benzalkonium Chloride
Biodegradability of chlorhexidine (CH), triclosan (TC), and benzalkonium chloride (CBA) has been tested in 18 surface water sampling points in the urban area of Buenos Aires. Sampling points were located in both the Reconquista and the Matanza-Riachuelo basins as well as in the La Plata River. High tolerance to the three disinfectants was found and indigenous strains capable of degrading CBA and TC were isolated. Neither tolerance nor biodegradation were correlated with sewage pollution. A strain that degrades CBA was identified as belonging to the genus Pseudomonas using the API20NE system and 16SRNA sequencing. In batch assays, the strain was capable of degrading 100, 200, and up to 500 mg L−1 of CBA in 10, 25, and 46 h respectively with specific growth rates (μ) of 0.56, 0.30, and 0.14 h−1. The efficiency of the process was between 99.5–98.0% in terms of compound removal and between 93.8–89.1% in terms of chemical oxygen demand (COD). The detoxification of the compound as a result of the biodegradation was assessed using Pseudokirchneriella subcapitata, Vibrio fischeri, and Lactuca sativa as test organisms.
KeywordsBenzalkonium chloride Triclosan Chlorhexidine Pseudomonas Biodegradation Detoxification
We also thank Dr. Gabriel Gutkind and Dr. Marcela Radice from the Laboratory of Bacterial Resistance, Facultad de Farmacia y Bioquímica, Universidad de Buenos Aires, for his collaboration in the identification of microorganisms.
We thank the University of Buenos Aires for the grant given for this study, supported by UBACYT Program-Project 20020130100378BA 2014-2017.
- ACUMAR (2015). Base de datos hidrológica-Cuenca Matanza Riachuelo. BDH-CMR http://www.bdh.acumar.gov.ar:8081/bdh3/aguasuperficial_listado.php Accessed 27 March 2017.
- Alexander, M. (1999). Biodegradation and bioremediation (2nd ed.). London: Academic Press.Google Scholar
- APHA-American Public Health Association, American Water Works Association, Water Environment Federation. (2012). Standard methods for the examination of water and wastewater (22nd ed.). Washington, DC: APHA.Google Scholar
- Baroni, S., Calcagno, M. L., Fortunato, M. S., Álvarez Roncancio, J. D., Gallego, A, & Korol, S. E. (2016) Evaluación de un método colorimétrico directo para la medición de cloruro de benzalconio. The Journal of the Argentine Chemical Society 103 (1–2), https://www.aqa.org.ar/images/anales/pdf103/cd/01-Qca-Analitica/01-008.PDF. Accessed 10 February 2017.
- Dougherty, J. A., Swarzenski, P. W., Dinicola, R. S., & Reinhard, M. (2010). Occurrence of herbicides and pharmaceutical and personal care products in surface water and groundwater around Liberty Bay, Puget Sound, Washington. Journal of Environmental Quality, 39(4), 1173–1180. https://doi.org/10.2134/jeq2009.0189.CrossRefGoogle Scholar
- Freitag, D., Geyer, H., Kraus, A., Viswanathan, R., Kotzias, D., Attar, A., et al. (1982). Ecotoxicological profile analysis: VII. Screening chemicals for their environmental behavior by comparative evaluation. Ecotoxicology and Environmental Safety, 6(1), 60–81 0147–6513/82/010060–22$02.00/0.CrossRefGoogle Scholar
- EPA (Environmental Protection Agency) (1989). Protocols for short term toxicity screening of hazardous waste sites. A.8.7. Lettuce root elongation (Lactuca sativa). EPA 600/3-88/029. Washington, DC: U.S. Environmental Protection AgencyGoogle Scholar
- EPA (2017). PBTprofiler http://www.pbtprofiler.net. Accessed 6 February 2017.
- Fortunato, M. S., Fuentes Abril, N. P., Martinefsky, M., Trípodi, V., Papalia, M., Rádice, M., et al. (2016). Aerobic degradation of ibuprofen in batch and continuous reactors by an indigenous bacterial community. Environmental Technology, 37(20), 2617–2626. https://doi.org/10.1080/09593330.2016.1156773.CrossRefGoogle Scholar
- ISO 11348-3 (1998). Water quality. Determination of the inhibitory effect of water samples on the light emission of Vibrio fischeri (Luminescent bacteria test). Geneva: SwitzerlandGoogle Scholar
- ISO 8692 (2004). Water quality. Freshwater algal growth inhibition test with unicellular green algae. Polski Komitet Normalizacyjny: PolskaGoogle Scholar
- Khan, A. H., Topp, E., Scott, A., Sumarah, M., Macfie, S. M., & Ray, M. B. (2015). Biodegradation of benzalkonium chlorides singly and in mixtures by a Pseudomonas sp. isolated from returned activated sludge. Journal of Hazardous Materials, 299, 595–602. https://doi.org/10.1016/j.jhazmat.2015.07.073.CrossRefGoogle Scholar
- Korol, S., Orsingher, M., Santini, P., Moretton, J., & D’Aquino, M. (1989). Biodegradation of phenolic compounds, II. Effects of inoculum, xenobiotic concentration and adaptation on Acinetobacter and Pseudomonas phenol degradation. Revista Latinoamericana de Microbiología, 31(2), 117–120.Google Scholar
- Kümmerer, K., Eitel, A., Braun, U., Hubner, P., Daschner, F., Mascart, F., et al. (1997). Analysis of benzalkonium chloride in the effluent from European hospitals by solid-phase extraction and high-performance liquid chromatography with post-column ion-pairing and fluorescence detection. Journal of Chromatography A, 774(1–2), 281–286. https://doi.org/10.1016/S0021-9673(97)00242-2.CrossRefGoogle Scholar
- Lara Martín, P. A., Li, X., Bopp, R. F., & Brownawell, B. J. (2010). Occurrence of alkyltrimethylammonium compounds in urban estuarine sediments: behentrimonium as a new emerging contaminant. Environmental Science & Technology, 44(19), 7569–7575. https://doi.org/10.1021/es101169a.CrossRefGoogle Scholar
- Li, X., Luo, X., Mai, B., Liu, J., Chen, L., & Lin, S. (2014). Occurrence of quaternary ammonium compounds (QACs) and their application as a tracer for sewage derived pollution in urban estuarine sediments. Environmental Pollution, 185, 127–133. https://doi.org/10.1016/j.envpol.2013.10.028.CrossRefGoogle Scholar
- Loveira, E., Fiol, P., Senn, A., Curutchet, G., Candal, R., & Litter, M. (2012). TiO2-photocatalytic treatment coupled with biological systems for the elimination of benzalkonium chloride in water. Separation and Purification Technology, 91, 108–116. https://doi.org/10.1016/j.seppur.2011.12.007.CrossRefGoogle Scholar
- Martínez-Carballo, E., Sitka, A. L., Gonzalez-Barreiro, C., Kreuzinger, B. N., Fürhackerc, M., Scharf, S., et al. (2007a). Determination of selected quaternary ammonium compounds by liquid chromatography with mass spectrometry. Part I. Application to surface, waste and indirect discharge water samples in Austria. Environmental Pollution, 145(2), 489–496. https://doi.org/10.1016/j.envpol.2006.04.03.CrossRefGoogle Scholar
- Martínez-Carballo, E., González Barreiro, C., Sitka, A., Kreuzinger, N., Scharf, S., & Gans, O. (2007b). Determination of selected quaternary ammonium compounds by liquid chromatography with mass spectrometry. Part II. Application to sediment and sludge samples in Austria. Environmental Pollution, 146(2), 543–547. https://doi.org/10.1016/j.envpol.2006.07.016.CrossRefGoogle Scholar
- Natale, O. E. (2005). Water quality indicators for the La Plata River basin. Vienna: IWG-Environmental International Work Session on Water Statistics http://unstats.un.org/unsd/environment/envpdf/pap_wasess5a3laplatariver.pdf. Accessed 6 March 2017.Google Scholar
- OECD 301D. (1992). Guidelines for testing of chemicals. Closed bottle test. Paris: Organisation of Economic Cooperation and Development.Google Scholar
- Rosal, R., Rodríguez, A., Perdigón-Melón, J. A., Petre, A., García-Calvo, E., Gómez, M. J., et al. (2010). Occurrence of emerging pollutants in urban wastewater and their removal through biological treatment followed by ozonation. Water Research, 44(2), 578–588. https://doi.org/10.1016/j.watres.2009.07.004.CrossRefGoogle Scholar
- Sütterlin, R., Coker, A., & Kümmerer, K. (2008a). Mixtures of quaternary ammonium compounds and anionic organic compounds in the aquatic environment: elimination and biodegradability in the closed bottle test monitored by LC–MS/MSH. Chemosphere, 72(3), 479–484. https://doi.org/10.1016/j.chemosphere.2008.03.008.CrossRefGoogle Scholar
- Sütterlin, H., Alexy, R., & Kümmerer, K. (2008b). The toxicity of the quaternary ammonium compound benzalkonium chloride alone and in mixtures with other anionic compounds to bacteria in test systems with Vibrio fischeri and Pseudomonas putida. Ecotoxicology and Environmental Safety, 71(2), 498–505. https://doi.org/10.1016/j.ecoenv.2007.12.015.CrossRefGoogle Scholar
- Tandukar, M., Oh, S., Tezel, U., Konstantinidis, K. T., & Pavlostathis, S. G. (2013). Long-term exposure to benzalkonium chloride disinfectants results in change of microbial community structure and increased antimicrobial resistance. Environmental Science Technology, 47(17), 9730–9738. https://doi.org/10.1021/es401507k.CrossRefGoogle Scholar
- Zhang, C., Cui, F., Zeng, G. M., Jiang, M., Yang, Z. Z., Yu, Z. G., et al. (2015). Quaternary ammonium compounds (QACs): a review on occurrence, fate and toxicity in the environment. Science of the Total Environment, 518-519, 352–362. https://doi.org/10.1016/j.scitotenv.2015.03.007.CrossRefGoogle Scholar